Phenotypic plasticity in the common snapping turtle (Chelydra serpentina): long-term physiological effects of chronic hypoxia during embryonic development

Abstract

Studies of embryonic and hatchling reptiles have revealed marked plasticity in morphology, metabolism, and cardiovascular function following chronic hypoxic incubation. However, the long-term effects of chronic hypoxia have not yet been investigated in these animals. The aim of this study was to determine growth and postprandial O2 consumption (V̇o2), heart rate (fH), and mean arterial pressure (Pm, in kPa) of common snapping turtles (Chelydra serpentina) that were incubated as embryos in chronic hypoxia (10% O2, H10) or normoxia (21% O2, N21). We hypothesized that hypoxic development would modify posthatching body mass, metabolic rate, and cardiovascular physiology in juvenile snapping turtles. Yearling H10 turtles were significantly smaller than yearling N21 turtles, both of which were raised posthatching in normoxic, common garden conditions. Measurement of postprandial cardiovascular parameters and O2 consumption were conducted in size-matched three-year-old H10 and N21 turtles. Both before and 12 h after feeding, H10 turtles had a significantly lower fH compared with N21 turtles. In addition, V̇o2 was significantly elevated in H10 animals compared with N21 animals 12 h after feeding, and peak postprandial V̇o2 occurred earlier in H10 animals. Pm of three-year-old turtles was not affected by feeding or hypoxic embryonic incubation. Our findings demonstrate that physiological impacts of developmental hypoxia on embryonic reptiles continue into juvenile life.

Embryonic hypoxia programmes postprandial cardiovascular function in adult common snapping turtles (Chelydra serpentina)

“…Chronic hypoxia during embryonic development has a profound effect on reptiles, changing the trajectory of phenotype maturation of multiple systems, with a pronounced impact on the cardiovascular system (Kam, 1993;Crossley et al, 2003;Crossley and Altimiras, 2005;Owerkowicz et al, 2009;Eme et al, 2011Eme et al, , 2013Eme et al, , 2014Enok et al, 2013;Tate et al, 2015Tate et al, , 2016Wearing et al, 2016). Over the past decade, our understanding of embryonic cardiovascular development in these species has improved markedly.…”

“…Over the past decade, our understanding of embryonic cardiovascular development in these species has improved markedly. However, very few studies have determined lasting impacts of morphological and physiological phenotypic modifications on juveniles and adults (Owerkowicz et al, 2009;Galli et al, 2016;Wearing et al, 2016). Much of the work that has been conducted so far has illustrated that embryonic reductions in oxygen availability restrict body mass at hatching (Kam, 1993;Crossley and Altimiras, 2005;Owerkowicz et al, 2009;Eme et al, 2011Eme et al, , 2013Eme et al, , 2014Marks et al, 2013;Tate et al, 2015Tate et al, , 2016Crossley et al, 2017b), and this persists into the first years of posthatching life (Owerkowicz et al, 2009;Galli et al, 2016;Wearing et al, 2016).…”

“…However, very few studies have determined lasting impacts of morphological and physiological phenotypic modifications on juveniles and adults (Owerkowicz et al, 2009;Galli et al, 2016;Wearing et al, 2016). Much of the work that has been conducted so far has illustrated that embryonic reductions in oxygen availability restrict body mass at hatching (Kam, 1993;Crossley and Altimiras, 2005;Owerkowicz et al, 2009;Eme et al, 2011Eme et al, , 2013Eme et al, , 2014Marks et al, 2013;Tate et al, 2015Tate et al, , 2016Crossley et al, 2017b), and this persists into the first years of posthatching life (Owerkowicz et al, 2009;Galli et al, 2016;Wearing et al, 2016). In addition, heart mass is relatively enlarged in embryonic reptiles chronically exposed to low oxygen (Kam, 1993;Crossley and Altimiras, 2005;Eme et al, 2013Eme et al, , 2014Marks et al, 2013;Tate et al, 2015Tate et al, , 2016, which again persists at least into the first years after hatching in American alligators (Owerkowicz et al, 2009;Galli et al, 2016), indicating that developmental hypoxia has a lasting impact on the cardiovascular phenotype of this species.…”

“…For reptiles, feeding elicits marked elevations in oxygen consumption rate ( _ V O 2 ) that last for several hours (Secor and Diamond, 1999;Hicks et al, 2000;Wang et al, 2001a;Overgaard et al, 2002a;Hicks and Bennett, 2004;Enok et al, 2013;Wearing et al, 2016). This postprandial increase in oxygen demand necessitates increased _ Q to sufficiently supply tissues with oxygen Secor et al, 2000;Wang et al, 2001a;Hicks and Bennett, 2004;Andersen et al, 2005;Secor and White, 2010;Enok et al, 2012Enok et al, , 2013Enok et al, , 2016Wearing et al, 2016). In terrestrial vertebrates, _ Q can be modulated by changes in heart rate ( f H ) and/or V S .…”

Eggshell structure in Caiman latirostris eggs improves embryo survival during nest inundation

“…As development occurs, the eggshell gets thinner [18] and the number and size of pores increases [19,20]. These changes could be adaptations to avoid hypoxia, as hypoxia reduces hatching success [21] and/or has subsequent adverse effects on hatchlings [22]. Furthermore, embryo tolerance to hypoxia changes during development [21].…”